Cogn Process
DOI 10.1007/s10339-007-0192-9
REVIEW
Short-distance navigation in cephalopods: a review and synthesis
Christelle Alves Æ Jean G. Boal Æ Ludovic Dickel
Received: 8 May 2007 / Revised: 19 September 2007 / Accepted: 21 September 2007
Marta Olivetti Belardinelli and Springer-Verlag 2007
Abstract This paper provides a short overview of the
scientific knowledge concerning short-distance navigation
in cephalopods. Studies in laboratory controlled conditions
and observations in the field provide converging evidence
that cephalopods use visual cues to navigate and demonstrate spatial memory. A recent study also provides the
first evidence for the neural substrates underlying spatial
abilities in cuttlefish. The functions of spatial cognition
in cephalopods are discussed from an evolutionary
standpoint.
Keywords Invertebrates Comparative cognition Spatial learning Hippocampus
Introduction
Cephalopod mollusks are a large and very successful taxonomic group. There are about 700 species living today
throughout the seas of the world. All living cephalopods
belong either to Nautiloidea, the representatives of ancient
cephalopods with an external shell, or to Coleoidea, the
C. Alves L. Dickel (&)
Laboratoire de Physiologie du Comportement des Céphalopodes,
E.A. 3211, Université de Caen Basse-Normandie,
Esplanade de la Paix, 14032 Caen cedex, France
e-mail: [email protected]
C. Alves L. Dickel
Centre de Recherches en Environnement Côtier,
Université de Caen, 54 rue du Dr. Charcot,
14530 Luc-sur-Mer, France
J. G. Boal
Department of Biology, Millersville University,
Millersville, PA 17551-0302, USA
modern cephalopods with an internal (or absent) shell. The
major orders of Coleoidea are the cuttlefishes, the squids
and the octopods. Cephalopod body structure and way of
life have changed dramatically over the course of their
evolution. Packard (1972) suggested that their evolution
was driven by selection pressures imposed by competition
with fishes.
Cephalopods possess all sophisticated organs required to
potentially solve the spatial problems they can be confronted with in their natural environment: efficient
locomotor effectors (powerful muscles of the mantle, funnel
and fins) associated with elaborate sense organs. These
sense organs rival the equivalent vertebrate systems in their
sophistication. First among cephalopod sense organs are
their well-developed eyes, which structurally resemble
those of vertebrates (with the lens, iris and retina; reviewed in Budelmann 1994). Cephalopods are color-blind
(Marshall and Messenger 1996; Mäthger et al. 2006), but
can discriminate the plane of polarization of light (Moody
and Parriss 1960; Shashar et al. 2000). Cephalopods also
have excellent tactile and chemical sensitivity in their
suckers (Graziadei 1964) and possess olfactory organs
below and behind their eyes functioning as chemoreceptors
(Gilly and Lucero 1992; Woodhams and Messenger 1974).
In addition, they have an elaborate equilibration system, the
statocysts, which can be compared to the vestibular system
of vertebrates (Stephen and Young 1982; Young 1960).
These sense organs provide information about gravity and
angular acceleration necessary for controlling equilibration.
Finally, cephalopods possess a system analogous to the
lateral line of fishes, which they use to detect water
movements (Budelmann and Bleckmann 1988).
In most modern cephalopods, a complex nervous system
with a complex and multi-lobed central brain has evolved
(reviewed in Nixon and Young 2003). The brain of
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octopuses and cuttlefishes is enclosed in a cartilaginous
cranium and lies between the eyes. The gut passes through
the brain and divides it into supra- and sub-oesophageal
masses that lie between two large optic lobes (Fig. 3a, b).
The brain-to-body ratio is large, somewhere between that
of fishes and reptiles and that of birds and mammals
(Packard 1972). This complex nervous system allows
cephalopods to display good performance in a wide range
of learning (reviewed in Sanders 1975; Mather 1995),
including associative learning (e.g., Agin et al. 2006a;
Darmaillacq et al. 2004), discriminative learning (e.g.,
Boal 1996; Cole and Adamo 2005), observational learning
(Fiorito and Scotto 1992; but see Biederman and Davey
1993; Suboski et al. 1993) and imprinting (Darmaillacq
et al. 2006). These learning abilities are associated with
significant long-term memory abilities (e.g., several weeks’
retention of a discrimination task in Octopus vulgaris,
Sanders 1970; reviewed in Agin et al. 2006b; Sanders
1975). Extraordinary behavioral plasticity has been
observed for communication, predation and defense
(e.g., Poirier et al. 2004, 2005; reviewed in Hanlon and
Messenger 1996).
For cephalopods, as for other moving animals, knowing
the spatial structure of the environment should be of prime
importance for avoiding predators, searching for food,
finding their way back home or remembering the location
of conspecifics. This hypothesis for the existence of spatial
abilities in cephalopods has led to a growing interest in
studying spatial cognition in these mollusks; however,
there is currently no existing review on cephalopods’
spatial navigation. This paper aims to provide an overview
of current scientific knowledge concerning short-distance
navigation in cephalopods. In the first section, we present
evidence of cephalopods’ spatial abilities under controlled
laboratory conditions. In the second section, we present an
overview of mechanisms that cephalopods have evolved to
deal with spatial tasks. Only studies of octopuses and
cuttlefishes are presented because there are little data
available addressing squids. In the last section, we will
review field evidence addressing the functions of spatial
cognition in cephalopods from an evolutionary standpoint.
Laboratory evidence for spatial abilities in cephalopods
Detour experiments
Detour behavior is the ability of an animal to reach a
stimulus (a goal) when there is an obstacle between the
subject and the stimulus (Zucca et al. 2005). Detour
behavior is a cognitively challenging task; it suggests that
the animal must maintain a spatial representation of the
location of the goal after abandoning a clear view of it.
After repeated trials, an animal does not need any kind of
spatial representation to complete a detour, however,
because the animal can learn ‘‘how’’ to reach the goal: this
is called detour learning. For example, the animal can learn
associations between particular environmental stimuli and
motor responses (e.g., ‘‘I turn right, the prey is no longer
visible, but if I then turn left, I will see it again’’).
Detour behavior is likely to be needed by cephalopods to
negotiate obstacles when hunting in their natural surroundings. Laboratory studies by Schiller (1949) and Wells
(1964) tested the abilities of O. vulgaris to solve a detour
task and explored the strategies the octopuses used. In both
experiments, octopuses were trained to detour around
opaque partitions to reach a crab visible behind a transparent wall, but not directly accessible to them (Fig. 1). In
Wells’ experiment (1964), only eight octopuses out of 29
succeeded in solving the detour problem in the first trial.
The failure of the majority of the octopuses could be
interpreted as demonstrating an inability to show detour
behavior, and hence an absence of spatial representation in
octopuses. However, Regolin et al. (1994) showed that in
Fig. 1 Schematic
representation of the detour
maze used in Wells’
experiments (modified from
Wells 1964)
Transparent wall
Opaque wall
Crab in a glass jar
C
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H
C
Choice compartment
H
Home compartment
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chicks, performances in detour problems can be affected by
perceptual and motivational factors. In the experiments of
Schiller (1949) and Wells (1964), the transparent wall that
separated the octopuses from the crabs could have been
such an unnatural stimulus that the animals failed to perceive it as an obstacle. With repeated trials, the octopuses
showed some improvement in performance, spending less
time attacking through the glass before entering the central
alley, and all animals learned to complete the task. But
what did the octopuses learn? Schiller (1949) suggested
that octopuses needed to maintain constant tactile contact
with the wall separating them from the goal. Wells later
showed (1964) that if the tactile contact was lost, the
octopuses needed to maintain a continuous visual fixation
on the wall. Thus, detour behavior in octopuses was visually guided; bodily position was not used to compute
position of the goal relative to their body. These detour
experiments did not provide clear evidence for spatial
representation in octopuses; however, they did show that
octopuses can develop an efficient strategy to solve a
spatial task.
Maze experiments
According to O’Keefe and Nadel (1978), exploratory
behavior permits an animal to build a spatial representation
of a new environment. Boal and colleagues asked whether
cephalopods would explore an unfamiliar environment to
gain a knowledge of the surroundings. First, Boal et al.
(2000) examined spontaneous locomotor activity in O.
bimaculoides when placed in a new environment. A gradual decrease in activity was observed over 3 days. Then,
the authors tested the octopuses to determine if the reduced
movement was associated with learning. They placed
octopuses for a period of 23 h in a new environment with
two burrows, only one open. After a resting period of 24 h,
the octopuses were returned to the testing tank. The results
showed that 16 out of 24 octopuses touched the previously
open burrow first. This result was interpreted as demonstrating exploratory learning in octopuses. In a more recent
investigation, preliminary tests undertaken by Karson et al.
(2003) strongly suggested that the cuttlefish Sepia officinalis also moved around a new environment to learn about
its features. These data bring the first evidence of a natural
propensity in cephalopods to explore their environment;
such behaviour is usually considered as a natural manifestation of spatial learning (Gallistel 1993; O’Keefe and
Nadel 1978).
Maze experiments have been undertaken by several
authors to reveal cephalopods’ abilities to solve spatial
tasks. The first maze experiment was conducted by Walker
et al. (1970). The authors trained O. maya in a dry T-maze
apparatus. The octopuses had to learn to enter a goal
compartment to regain access to seawater. They were
trained for 27 days with three trials a day to enter the goal
compartment opposite to their initial side-turning preference. At the end of training, all octopuses were performing
without errors. This experiment provided convincing evidence of maze learning ability in octopuses. Later, Boal
et al. (2000) designed another spatial task comparable to a
natural spatial problem. The authors trained O. bimaculoides, in about 20 trials, to relocate an open escape burrow
among six possible locations around the periphery of a
round arena. Octopuses quickly learned the location of the
open burrow (i.e., improved performances after only three
trials), and were able to remember the location for a week.
In a more recent study, Karson et al. (2003) addressed
whether cuttlefish, S. officinalis, also display good maze
learning abilities in a visual–spatial discrimination task.
The authors trained cuttlefish to exit a round arena with two
exit holes surrounded by visual cues, only one exit hole
being opened. Cuttlefish learned the task in a mean of 36
trials. Most recently, both octopuses and cuttlefish demonstrated the ability to solve two separate maze problems
when trials with the two mazes were intermixed (Hvorecny
et al. 2007). Taken together, these studies show that spatial
learning is well within the abilities of at least some species
of octopuses and cuttlefishes. Even if these maze experiments have not studied which sensory senses and spatial
mechanisms cephalopods use to orient, they began to
reveal the kinds of spatial tasks octopuses and cuttlefish are
able to solve.
Mechanisms of spatial abilities in cephalopods
Use of chemical cues
Detection of chemical cues can be either through distant or
contact chemoreception. Several studies have showed that
octopuses and cuttlefish are capable of distance chemoreception (Lee 1992; Boal and Golden 1999). Detection of the
spatial gradient of chemical cues in water could be a way for
cephalopods to orient; unfortunately, there is no data yet
available in the literature addressing this possibility. Among
mollusks, a common way of returning to a place is to secrete
a chemical trail on a solid substrate while leaving and then
retrace that trail when returning. This strategy is called trail
following and depends on contact chemoreception. Mather
(1991a) and Forsythe and Hanlon (1997) recorded hunting
paths of O. vulgaris and O. cyanea, respectively, in their
natural environment (Fig. 2a, b). For long distance trips,
octopuses traveled by jetting through the water when
leaving (Mather 1991a) or returning home; consequently,
they were not in contact with the substrate. Furthermore, the
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Cogn Process
Fig. 2 Schematic representation of foraging trips. a Successive hunts numbered from 1 to 7 of a juvenile Octopus vulgaris (from Mather 1991).
b Successive hunts of two specimen (J and R) of Octopus cyanea (from Forsythe and Hanlon 1997)
octopuses did not retrace their outgoing paths when they
returned. In O. vulgaris, the trail overlap was only 32%
(Mather 1991a). Finally, in both studies, the octopuses
sometimes made tortuous hunting paths, and then swam
directly back to their den afterward. Based on these data, the
authors rejected the hypothesis of trail following in octopuses and suggested that octopuses have accurate
knowledge of the seascape. No study yet supports trail
following in octopuses; however, this absence of evidence
does not exclude the possibility that octopuses could use
this strategy in particular environmental conditions (low
visibility, for example).
Use of visual cues
Single landmark
The complexity of cephalopods’ visual system and their
high performances in visual discrimination tasks (cuttlefish: Cole and Adamo 2005; octopuses: Boal 1996; Wells
1978) suggest that cephalopods could use visual landmarks
to orient. Landmarks can be used in a variety of ways to
provide information about the location of the goal. For
example, an animal can learn to go to a particular landmark
(a beacon) marking the location of a goal, regardless of the
motor behavior involved. This behavior can be called
landmark guidance, beaconing (Gallistel 1993) or stimulusapproach behavior (Schmajuk and Thieme 1992). An animal can also use the configuration of several landmarks to
localize the goal; this behavior can be called piloting
(Gallistel 1993).
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A series of laboratory experiments investigating cephalopods’ ability to use visual landmarks to orient were
carried out by Mather (1991a) using octopuses. First, this
author trained octopuses (O. rubescens) to go to a piece of
plastic tubing (the beacon) to find a food reward located
within a featureless circular tank. Mather showed that the
octopuses learned to approach the plastic tubing even when
it was moved around the tank. These results showed
octopuses’ ability to rely on a single landmark to label the
location of a goal. Interestingly, Mather also showed that
when a box and a dish were added in the tank, the octopus
moved first to the larger landmark (the box), and next,
oriented to the plastic tubing associated with food. We can
interpret such results as learning a stimulus-approach
association when a single landmark is available (beaconing), and possibly learning stimulus-approach behaviors
linked together in chains to compose a route when several
landmarks are available. Results were not definitive,
however, for either orienting using landmarks in chains or
for orienting using the geometrical relationships between
landmarks. Simplified strategies such as use of landmarks
in chains are widespread in other invertebrates, such as
arthropods. Ants learn and recognize landmarks distributed
along a route, and they correct their course relative to these
landmarks (Collett et al. 1992). It would be interesting to
study if the same strategy has evolved in cephalopods.
In a second experiment, Mather (1991a) tested whether
octopuses rely on visual landmarks to find the entrance of
their den in their natural environment (stimulus-approach
behavior or beaconing). The author used the transformational approach, a common experimental technique
pioneered by Tinbergen (reviewed in Cheng and Spetch
Cogn Process
1998). Changing different aspects of the environment is a
common tool used to understand which cues an animal
relies on. Mather (1991a) placed artificial landmarks
around the entrance of the den of several O. vulgaris. After
2 days, the author displaced the landmarks one meter away.
The returning octopuses went directly to their homes,
appearing to rely on more conspicuous and stable natural
landmarks. We can hypothesize, then, that a visual landmark that is stable and more accurate or reliable across
time is more likely to be used by octopuses.
Alternatively, the octopuses could have been using a
strategy called path integration. Path integration allows
animals to deduce their position relative to their starting
point (direction and distance) from their own movements
and then use this information to return home directly after a
tortuous path. This strategy occurs very widely in the
animal kingdom, from arthropods to humans (ants: Wehner
2003; crabs: Layne et al. 2003; mammals: Etienne et al.
1996), and could have also evolved in octopuses.
strategy to solve the maze. This study revealed cuttlefishes’
spontaneous behavioral flexibility in solving a spatial task.
An animal using the configuration of several landmarks
to localize its goal (piloting) relies on geometric properties
such as distances, angles or directions. Although no study
has yet attempted to directly test the piloting hypothesis in
cephalopods, Mather (1991b) provided some interesting
preliminary observations. When octopuses hunt, they can
consume their prey at the capture site or they can bring it
back to their den to consume it. Mather (1991b) showed
that the greater the distance between the capture site and
the home den, the more likely the octopus was to eat the
prey where it had been caught. The author interpreted this
result in two ways: the octopus could have made an estimation of its distance to home using the energy it had
expended as it moved out to forage, or the octopus could
have spatial knowledge of the surroundings of its den.
Spatial memory and neural substrates
Multiple landmarks
The cross-maze spatial task has been extensively used to
explore spatial learning strategies in a wide range of
models (rats: Restle 1957; fish: Odling-Smee and Braithwaite 2003). This procedure allows the authors to ask
several questions: do the animals use the array of visual
cues (place strategy) to solve the maze? Or do they use a
body-centered algorithmic behavior (list of instructions
such as ‘‘turn left…’’; response strategy)? Karson (2003)
demonstrated that cuttlefish could be trained to exit a
round, open maze using proximal visual cues (which could
be a form of place strategy), right/left orientation (response
strategy), or a combination of both types of cues. Alves
et al. (2007) designed a spatial learning procedure using a
cross-maze to test, which strategy cuttlefish used spontaneously. They devised cross-mazes with either proximal
visual cues (just above the surface of the water) or distal
visual cues (around the testing room). In these mazes, the
cuttlefish S. officinalis learned to enter a dark and sandy
compartment at the end of a goal arm in a mean of 25 trials.
After acquisition of this task, the authors created a conflict
between the algorithmic behavior (response strategy) and
the visual cues identifying the goal (place strategy). When
cuttlefish were trained with distal visual cues, most of them
relied on response strategy, and when trained with proximal visual cues, the two strategies were used equally often.
These results confirmed the existence of both response and
place strategies in cuttlefish, similar to results described in
vertebrates (e.g., Gibson and Shettleworth 2005). Moreover, the availability and salience of visual cues seemed to
determine whether the cuttlefish used the response or place
Two kinds of spatial memory have been commonly distinguished in the literature: reference spatial memory and
working spatial memory. Reference spatial memory
encodes spatial information that is likely to remain stable
and reliable across time. In contrast, working spatial
memory is retained only long enough to complete a particular task, after which the information is discarded,
presumably because it is no longer needed. Both Mather’s
studies (O. vulgaris, 1991a, b) and Forsythe and Hanlon’s
study (O. cyanea; 1997) showed that octopuses hunted in
several different directions around their home on successive hunts and even on successive days (Fig. 2a, b). Based
on her observations, Mather (1991a) suggested the existence of working spatial memory in octopuses for where
they had already hunted. Reference spatial memory in
octopuses could refer to the spatial knowledge of the
surroundings.
The vertical lobe complex is a highly associative
structure of the cephalopods’ central nervous system. It is
situated in the extreme dorsal part of the supra-oesophageal
mass. This complex consists of several lobes closely
interconnected: the vertical (VL), superior frontal and
subvertical lobes (Fig. 3b). The vertical complex has been
structurally compared to the hippocampus of vertebrates
(Young 1991). Neural networks in both structures consist
of sequences of matrices with numerous interacting channels. Parallel pathways are mutually reinforcing (Young
1991). Hochner et al. (2003) found that the VL of octopuses manifests long-term potentiation similar to that
observed in the hippocampus of vertebrates. Thus, the VL
is a structure of particular interest for studies of the neural
substrates of spatial learning mechanisms in cephalopods.
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Fig. 3 Photomicrographs of the central nervous system of Sepia officinalis. a Frontal section (scale bar 1 mm). b Sagittal section (scale bar
500 lm). oe Oesophagus, OL optic lobe, VL vertical lobe, SV subvertical lobe, Fs superior frontal lobe
Graindorge et al. (2006) have made electrolytic lesions in
either the ventral or the dorsal parts of the VL in cuttlefish
S. officinalis. Sham-operated and VL lesioned cuttlefish
were trained in a spatial learning procedure using a T-maze
and were tested in an open field. The results showed that
ventral lesions of the VL led to impairment in the acquisition of spatial tasks whereas dorsal lesions increased
locomotor activity in an open field. This research established for the first time functional analogies between the
VL and the hippocampus (locomotor activity level and
memory). Future studies will address more precisely the
function of the VL in spatial learning.
Behavioral ecology of spatial abilities in cephalopods
Space utilization in cephalopods
Field studies have been undertaken to better understand
space utilization in octopuses. Many octopuses spend most
of their time in protective shelters (reviewed in Boyle
1983, 1987). Depending on the species, they use several
types of dens, also called ‘‘homes’’, including holes in the
hard substratum (O. cyanea; Forsythe and Hanlon 1997),
sheltered niches under rocks (O. dofleini; Hartwick et al.
1978), within mollusk shells (O. joubini; Mather 1982),
and in rocks or litter of human origin (O. vulgaris;
Katsanevakis and Verriopoulos 2004). Octopuses can also
extensively modify a site by digging out sand and moving
rocks (O. bimaculatus; Ambrose 1982; O. vulgaris, Mather
1994). An octopus can occupy the same den over a period
of days (O. cyanea; Forsythe and Hanlon 1997; O. vulgaris; Mather and O’Dor 1991), weeks (O. cyanea; Yarnall
1969; O. dofleini; Hartwick et al. 1984; Mather et al. 1985;
O. vulgaris; Mather 1988) or even months (O. bimaculatus;
Ambrose 1982), after which it shifts to a new den. Occupancy duration is linked to den size and possibly the
presence of preferred prey (Mather 1994).
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Laboratory studies showing exploratory behavior in
octopuses (see above) suggest that we could expect octopuses to either explore a new area and then choose the best
place for its new den, or quickly choose a new den and
afterwards explore their surroundings. Mather (1994)
observed O. vulgaris as they foraged and stopped to choose
a new den; they explored little before choosing the dens
and their homes were subsequently extensively modified.
The author suggested that octopuses are always evaluating
and exploring new areas to gain knowledge of their
environment.
Octopuses are considered to be central place foragers
(Mather 1991a, b). Mather and O’Dor (1991) studied the
hunting trips of juvenile O. vulgaris off the coast of Bermuda and showed that the octopuses (49–115 g) hunted in
a circular area (15 m in diameter) centered approximately
on their den. In a related study, juvenile octopuses routinely hunted away from their dens on complicated trips
that averaged 55 min in duration and 9.3 m in distance
(Mather 1991a). Forsythe and Hanlon (1997) recorded
hunting paths of O. cyanea (300–700 g). Trips for these
octopuses averaged 118 min in duration and up to 120 m in
distance. Some spatial abilities must have evolved in
octopuses to allow them to find their way back home after
each of these hunting trips and, potentially, allow them to
remember the distribution of food patches and already
depleted areas.
Cuttlefishes are thought to rely primarily on crypsis for
defense (Boletzky 1983; Hanlon and Messenger 1988).
They can dig into the sand for concealment (Mather 1986)
and they can also change the color and texture of their skin
to match the background. Aitken et al. (2005) have suggested that the giant Australian cuttlefish, S. apama, may
also use dens. The authors used a Radio Acoustic Positioning and Telemetry system (RAPT) to monitor cuttlefish
movements. During the first few days of monitoring, cuttlefish were continuously detected with the tracking system
(continuous data were obtained); thereafter, there was a
Cogn Process
strong reduction in quantity of data obtained. The authors
suggested that the cuttlefish may have been hiding in dens
(rock crevice, no signal), and sometimes going out to hunt
(signals). From these observations alone, we cannot
determine if each cuttlefish was using a single shelter from
1 day to another or multiple different shelters, and if
sheltering is a widespread behavior in cuttlefishes. Aitken
et al. (2005) also showed high site fidelity in individual S.
apama, with cuttlefish confining their hunting to a restricted area. We can hypothesize, therefore, that cuttlefishes,
like octopuses, may have spatial knowledge of their surroundings at least to optimize their hunting time.
In many animals, spatial abilities also appear to be
crucial for social behaviors. In cephalopods, both octopuses
and cuttlefishes are generally considered to be solitary,
except during reproduction (Boal and Golden 1999;
Yarnall 1969). Octopuses typically avoid each other. In O.
vulgaris, Altman (1967) observed dens close together but
there were no signs of interactions between neighbors. In
O. cyanea, after visual contact, one octopus slowly
extended an arm to make physical contact, after which the
other octopus typically swam off (Yarnall 1969; Forsythe
and Hanlon 1997). In Abdopus aculeatus, Huffard (2007)
observed individual males occupying dens adjacent to
those of particular females. The males mate-guarded and
copulated repeatedly with the adjacent female for multiple
days. There is yet no clear evidence of an octopus consistently defending its home range against conspecifics,
however; thus, most authors consider that octopuses are
non-territorial.
Cuttlefishes are considered to be solitary for the major
part of their life cycle. They seem to tolerate conspecifics
without being attracted by them. In S. apama, the giant
Australian cuttlefish, a large spawning aggregation occurs
every winter over a restricted area of rocky reef in South
Australia (Hall and Hanlon 2002). Some aspects of their
complex mating system have been compared with those of
leks. It is not known how cuttlefish find their way to
spawning aggregations, and it remains to be determined
whether group stability in any cephalopod species depends
on social recognition between individuals or on spatial
learning (reviewed in Boal 2006).
Spatial abilities and cephalopods’ life styles
Cephalopods are considered to have a ‘‘live fast and die
young’’ life-style (O’Dor and Webber 1986); they grow
quickly, and few of them live more than 2 years (reviewed
in Boyle 1983, 1987). They are also exposed to strong
competition and predation pressures. It appears reasonable
to assume that spatial learning abilities must have evolved
to allow them to spend a minimum amount of time exposed
to predators while foraging. The evolution of cephalopods
is closely linked to the reduction and internalization of the
shell (Ward and Bandel 1987). In the benthic, cryptic
cuttlefishes, the shell is mainly implicated in buoyancy
regulation (Birchall and Thomas 1983). In the fast-moving
squids, a cartilaginous pen is all that remains of the shell,
and it serves as a support for musculature. In the secretive
octopuses, the shell has almost disappeared, allowing them
to hide in small crevices or holes in the substrate. These
evolutionary trajectories demonstrate clear connections
between morphology and behavior, with each group
adapting with one of the defensive strategies typically
described for cephalopods: camouflage, escape or shelter
occupancy. Consequently, it is likely that each group of
cephalopods has faced specific spatial problems and has
evolved specific spatial strategies.
Cephalopods are found in a wide range of aquatic habitats; for example, some live in visually rich coral reefs
while others live in the surface waters, or in the deep ocean
where little or no light penetrates. Even within a species,
populations may not share identical environmental conditions. It is reasonable to hypothesize, therefore, that
cephalopods have evolved a large array of adaptive spatial
strategies. Future studies that facilitate between- and
within-species comparisons will provide a better understanding of the genetic and ecological components of
variation in spatial abilities. Comparisons with other
invertebrate and vertebrate models, such as arthropods or
rodents, would also be important for understanding the
evolution of navigational strategies in the animal kingdom.
Conclusion
Tinbergen (1963) outlined four major questions that can be
asked in ethology. They are often categorized as proximate
explanations for behavior (causation and development)
or ultimate explanations for behavior (functions and
evolution).
At the proximate level, laboratory studies in controlled
conditions as well as observations in the field have yielded
clear evidence for spatial abilities and have provided some
evidence for the spatial mechanisms that cephalopods use
to orient. Multiple studies support the importance of visual
cues to navigation and the use of both response learning
and place learning strategies. Preliminary evidence suggests that the vertical lobe complex could be performing
functions analogous to the hippocampus of vertebrates.
Cephalopods’ sophisticated nervous and sensorimotor
systems may support a wide range of strategies. No study
has yet addressed developmental questions associated with
cephalopod spatial abilities. However, cephalopods appear
to be good biological models for such studies because of
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the wide range of habitats they exploit and their high
behavioral flexibility during ontogenesis (Dickel et al.
2000; Hanlon and Messenger 1988; Poirier et al. 2004,
2005). It remains for future studies to provide a more
complete understanding of orientation mechanisms in
cephalopods.
At the ultimate level, field studies of shallow water
octopuses support the hypothesis that the spatial abilities of
cephalopods are important in both defense and foraging.
While numerous studies have provided some data for
spatial orientation in octopuses, field data for cuttlefishes
and squids are largely lacking. Improved information about
the functions of spatial abilities in all three groups will
facilitate the understanding of spatial cognition from
comparative, ecological and evolutionary perspectives.
Acknowledgments The authors would like to thank Pr. Raymond
Chichery for its helpful comments on the manuscript.
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